Human natural killer-1 sulfotransferase (HNK-1ST)-induced sulfate transfer regulates laminin-binding glycans on α-dystroglycan

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30823-30832

  Nakagawa, Naoki ^a   Manya, Hiroshi ^b   Toda, Tatsushi ^c   Endo, Tamao ^b   Oka, Shogo ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Tokyo Metropolitan Institute of Gerontology   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-TUMOR AGENTS; CANCER CELLS; CELL MIGRATION; GLYCANS; LIGAND BINDING ACTIVITY; MELANOMA CELLS; MOLECULAR MECHANISM; RETINOIC ACIDS; SULFATE GROUPS; TUMOR SUPPRESSION; TUMOR SUPPRESSORS; UP-REGULATION;

CELLS; CYTOLOGY; DERMATOLOGY; ESTERIFICATION; GLYCOSYLATION; ONCOLOGY; TUMORS;

SULFUR COMPOUNDS;

ALPHA DYSTROGLYCAN; HUMAN NATURAL KILLER 1 SULFOTRANSFERASE; LAMININ BINDING PROTEIN; MUTANT PROTEIN; RETINOIC ACID; SULFATE; SULFOTRANSFERASE; SULFUR 35; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; ATTENUATION; BINDING AFFINITY; CANCER INHIBITION; CHO CELL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; LIGAND BINDING; MELANOMA CELL; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM;

ANIMALS; CELL MOVEMENT; CHO CELLS; CRICETINAE; CRICETULUS; DYSTROGLYCANS; GLYCOSYLATION; HUMANS; LAMININ; MUTATION; POLYSACCHARIDES; SULFOTRANSFERASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84865744996     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.363036     Document Type: Article

References (53)

1. Friedl, P., and Alexander, S. (2011) Cancer invasion and the microenvironment. Plasticity and reciprocity. Cell 147, 992-1009
2. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867
3. Fuster, M. M., and Esko, J. D. (2005) The sweet and sour of cancer. Glycans as novel therapeutic targets. Nat. Rev. Cancer 5, 526-542
4. Meany, D. L., and Chan, D. W. (2011) Aberrant glycosylation associated with enzymes as cancer biomarkers. Clin. Proteomics 8, 7
5. Hakomori, S. (1996) Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 56, 5309-5318
6. Zhao, X., Graves, C., Ames, S. J., Fisher, D. E., and Spanjaard, R. A. (2009) Mechanism of regulation and suppression of melanoma invasiveness by novel retinoic acid receptor-γ target gene carbohydrate sulfotransferase 10. Cancer Res. 69, 5218-5225
7. Morita, I., Kizuka, Y., Kakuda, S., and Oka, S. (2008) Expression and function of the HNK-1 carbohydrate. J. Biochem. 143, 719-724
8. Morita, I., Kakuda, S., Takeuchi, Y., Kawasaki, T., and Oka, S. (2009) HNK-1 (human natural killer-1) glyco-epitope is essential for normal spine morphogenesis in developing hippocampal neurons. Neuroscience 164, 1685-1694
9. Morita, I., Kakuda, S., Takeuchi, Y., Itoh, S., Kawasaki, N., Kizuka, Y., Kawasaki, T., and Oka, S. (2009) HNK-1 glyco-epitope regulates the stability of the glutamate receptor subunit GluR2 on the neuronal cell surface. J. Biol. Chem. 284, 30209-30217
10. Yamamoto, S., Oka, S., Inoue, M., Shimuta, M., Manabe, T., Takahashi, H., Miyamoto, M., Asano, M., Sakagami, J., Sudo, K., Iwakura, Y., Ono, K., and Kawasaki, T. (2002) Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J. Biol. Chem. 277, 27227-27231
11. Chou, D. K., Ilyas, A. A., Evans, J. E., Costello, C., Quarles, R. H., and Jungalwala, F. B. (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. J. Biol. Chem. 261, 11717-11725
12. Ariga, T., Kohriyama, T., Freddo, L., Latov, N., Saito, M., Kon, K., Ando, S., Suzuki, M., Hemling, M. E., and Rinehart, K. L., Jr. (1987) Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM M-proteins in patients with neuropathy. J. Biol. Chem. 262, 848-853
13. Kizuka, Y., Matsui, T., Takematsu, H., Kozutsumi, Y., Kawasaki, T., and Oka, S. (2006) Physical and functional association of glucuronyltransferases and sulfotransferase involved in HNK-1 biosynthesis. J. Biol. Chem. 281, 13644-13651
14. Terayama, K., Oka, S., Seiki, T., Miki, Y., Nakamura, A., Kozutsumi, Y., Takio, K., and Kawasaki, T. (1997) Cloning and functional expression of a novel glucuronyltransferase involved in the biosynthesis of the carbohydrate epitope HNK-1. Proc. Natl. Acad. Sci. U.S.A. 94, 6093-6098
15. Seiki, T., Oka, S., Terayama, K., Imiya, K., and Kawasaki, T. (1999) Molecular cloning and expression of a second glucuronyltransferase involved in the biosynthesis of the HNK-1 carbohydrate epitope. Biochem. Biophys. Res. Commun. 255, 182-187
16. Ong, E., Yeh, J. C., Ding, Y., Hindsgaul, O., and Fukuda, M. (1998) Expression cloning of a human sulfotransferase that directs the synthesis of the HNK-1 glycan on the neural cell adhesion molecule and glycolipids. J. Biol. Chem. 273, 5190-5195
17. Tagawa, H., Kizuka, Y., Ikeda, T., Itoh, S., Kawasaki, N., Kurihara, H., Onozato, M. L., Tojo, A., Sakai, T., Kawasaki, T., and Oka, S. (2005) A nonsulfated form of the HNK-1 carbohydrate is expressed in mouse kidney. J. Biol. Chem. 280, 23876-23883
18. Ibraghimov-Beskrovnaya, O., Ervasti, J. M., Leveille, C. J., Slaughter, C. A., Sernett, S. W., and Campbell, K. P. (1992) Primary structure of dystrophin- associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696-702
19. Barresi, R., and Campbell, K. P. (2006) Dystroglycan. From biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207
20. Han, R., Kanagawa, M., Yoshida-Moriguchi, T., Rader, E. P., Ng, R. A., Michele, D. E., Muirhead, D. E., Kunz, S., Moore, S. A., Iannaccone, S. T., Miyake, K., McNeil, P. L., Mayer, U., Oldstone, M. B., Faulkner, J. A., and Campbell, K. P. (2009) Basal lamina strengthens cell membrane integrity via the laminin G domain-binding motif of α-dystroglycan. Proc. Natl. Acad. Sci. U.S.A. 106, 12573-12579
21. Ervasti, J. M., Burwell, A. L., and Geissler, A. L. (1997) Tissue-specific heterogeneity in α-dystroglycan sialoglycosylation. Skeletal muscle α-dystroglycan is a latent receptor for Vicia villosa agglutinin b4 masked by sialic acid modification. J. Biol. Chem. 272, 22315-22321
22. Michele, D. E., and Campbell, K. P. (2003) Dystrophin-glycoprotein complex. Post-translational processing and dystroglycan function. J. Biol. Chem. 278, 15457-15460
23. Ervasti, J. M., and Campbell, K. P. (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823
24. Michele, D. E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R. D., Satz, J. S., Dollar, J., Nishino, I., Kelley, R. I., Somer, H., Straub, V., Mathews, K. D., Moore, S. A., and Campbell, K. P. (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418, 417-422
25. Muntoni, F., Torelli, S., and Brockington, M. (2008) Muscular dystrophies due to glycosylation defects. Neurotherapeutics 5, 627-632
26. Beltrán-Valero de Bernabé, D., Currier, S., Steinbrecher, A., Celli, J., van Beusekom, E., van der Zwaag, B., Kayserili, H., Merlini, L., Chitayat, D., Dobyns, W. B., Cormand, B., Lehesjoki, A. E., Cruces, J., Voit, T., Walsh, C. A., van Bokhoven, H., and Brunner, H. G. (2002) Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am. J. Hum. Genet. 71, 1033-1043
27. van Reeuwijk, J., Janssen, M., van den Elzen, C., Beltran-Valero de Bernabé, D., Sabatelli, P., Merlini, L., Boon, M., Scheffer, H., Brockington, M., Muntoni, F., Huynen, M. A., Verrips, A., Walsh, C. A., Barth, P. G., Brunner, H. G., and van Bokhoven, H. (2005) POMT2 mutations cause α-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J. Med. Genet. 42, 907-912
28. Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., Inazu, T., Mitsuhashi, H., Takahashi, S., Takeuchi, M., Herrmann, R., Straub, V., Talim, B., Voit, T., Topaloglu, H., Toda, T., and Endo, T. (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev. Cell 1, 717-724
29. Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura K., Kondo-Iida, E., Nomura, Y., Segawa, M., Yoshioka, M., Saito, K., Osawa, M., Hamano, K., Sakakihara, Y., Nonaka, I., Nakagome, Y., Kanazawa, I., Nakamura, Y., Tokunaga, K., and Toda, T. (1998) An ancient retrotransposal insertion causes Fukuyamatype congenital muscular dystrophy. Nature 394, 388-392
30. Brockington, M., Blake, D. J., Prandini, P., Brown, S. C., Torelli, S., Benson, M. A., Ponting, C. P., Estournet, B., Romero, N. B., Mercuri, E., Voit, T., Sewry, C. A., Guicheney, P., and Muntoni, F. (2001) Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin α2 deficiency and abnormal glycosylation of α-dystroglycan. Am. J. Hum. Genet. 69, 1198-1209
31. Longman, C., Brockington, M., Torelli, S., Jimenez-Mallebrera, C., Kennedy, C., Khalil, N., Feng, L., Saran, R. K., Voit, T., Merlini, L., Sewry, C. A., Brown, S. C., and Muntoni, F. (2003) Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of α-dystroglycan. Hum. Mol. Genet. 12, 2853-2861
32. Bao, X., Kobayashi, M., Hatakeyama, S., Angata, K., Gullberg, D., Nakayama, J., Fukuda, M. N., and Fukuda, M. (2009) Tumor suppressor function of laminin-binding α-dystroglycan requires a distinct α3-N- acetylglucosaminyltransferase. Proc. Natl. Acad. Sci. U.S.A. 106, 12109-12114
33. de Bernabé, D. B., Inamori, K., Yoshida-Moriguchi, T., Weydert, C. J., Harper, H. A., Willer, T., Henry, M. D., and Campbell, K. P. (2009) Loss of α-dystroglycan laminin binding in epithelium-derived cancers is caused by silencing of LARGE. J. Biol. Chem. 284, 11279-11284
34. Nakagawa, N., Izumikawa, T., Kitagawa, H., and Oka, S. (2011) Sulfation of glucuronic acid in the linkage tetrasaccharide by HNK-1 sulfotransferase is an inhibitory signal for the expression of a chondroitin sulfate chain on thrombomodulin. Biochem. Biophys. Res. Commun. 415, 109-113
35. Kanagawa, M., Nishimoto, A., Chiyonobu, T., Takeda, S., Miyagoe-Suzuki, Y., Wang, F., Fujikake, N., Taniguchi, M., Lu, Z., Tachikawa, M., Nagai, Y., Tashiro, F., Miyazaki, J., Tajima, Y., Takeda, S., Endo, T., Kobayashi, K., Campbell, K. P., and Toda, T. (2009) Residual laminin binding activity and enhanced dystroglycan glycosylation by LARGE in novel model mice to dystroglycanopathy. Hum. Mol. Genet. 18, 621-631
36. Spanjaard, R. A., Ikeda, M., Lee, P. J., Charpentier, B., Chin, W. W., and Eberlein, T. J. (1997) Specific activation of retinoic acid receptors (RARs) and retinoid X receptors reveals a unique role for RARγ in induction of differentiation and apoptosis of S91 melanoma cells. J. Biol. Chem. 272, 18990-18999
37. Barresi, R., Michele, D. E., Kanagawa, M., Harper, H. A., Dovico, S. A., Satz, J. S., Moore, S. A., Zhang, W., Schachter, H., Dumanski, J. P., Cohn, R. D., Nishino, I., and Campbell, K. P. (2004) LARGE can functionally bypass α-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat. Med. 10, 696-703
38. Patnaik, S. K., and Stanley, P. (2005) Mouse large can modify complex Nand mucinO-glycans on α-dystroglycan to induce laminin binding. J. Biol. Chem. 280, 20851-20859
39. Yamauchi, S., Mita, S., Matsubara, T., Fukuta, M., Habuchi, H., Kimata, K., and Habuchi, O. (2000) Molecular cloning and expression of chondroitin 4-sulfotransferase. J. Biol. Chem. 275, 8975-8981
40. Okuda, T., Mita, S., Yamauchi, S., Fukuta, M., Nakano, H., Sawada, T., and Habuchi, O. (2000) Molecular cloning and characterization of GalNAc 4-sulfotransferase expressed in human pituitary gland. J. Biol. Chem. 275, 40605-40613
41. Kanagawa, M., Saito, F., Kunz, S., Yoshida-Moriguchi, T., Barresi, R., Kobayashi, Y. M., Muschler, J., Dumanski, J. P., Michele, D. E., Oldstone, M. B., and Campbell, K. P. (2004) Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117, 953-964
42. Brockington, M., Torelli, S., Prandini, P., Boito, C., Dolatshad, N. F., Longman, C., Brown, S. C., and Muntoni, F. (2005) Localization and functional analysis of the LARGE family of glycosyltransferases. Significance for muscular dystrophy. Hum. Mol. Genet. 14, 657-665
43. Ong, E., Yeh, J. C., Ding, Y., Hindsgaul, O., Pedersen, L. C., Negishi, M., and Fukuda, M. (1999) Structure and function of HNK-1 sulfotransferase. Identification of donor and acceptor binding sites by site-directed mutagenesis. J. Biol. Chem. 274, 25608-25612
44. Girard, J. P., Baekkevold, E. S., and Amalric, F. (1998) Sulfation in high endothelial venules. Cloning and expression of the human PAPS synthetase. FASEB J. 12, 603-612
45. Mooy, C. M., Luyten, G. P., de Jong, P. T., Jensen, O. A., Luider, T. M., van der Ham, F., and Bosman, F. T. (1995) Neural cell adhesion molecule distribution in primary and metastatic uveal melanoma. Hum. Pathol. 26, 1185-1190
46. Thies, A., Schachner, M., Berger, J., Moll, I., Schulze, H. J., Brunner, G., and Schumacher, U. (2004) The developmentally regulated neural crest-associated glycotope HNK-1 predicts metastasis in cutaneous malignant melanoma. J. Pathol. 203, 933-939
47. Casado, J. G., Delgado, E., Patsavoudi, E., Durán, E., Sanchez-Correa, B., Morgado, S., Solana, R., and Tarazona, R. (2008) Functional implications of HNK-1 expression on invasive behavior of melanoma cells. Tumour Biol. 29, 304-310
48. Stalnaker, S. H., Hashmi, S., Lim, J. M., Aoki, K., Porterfield, M., Gutierrez- Sanchez, G., Wheeler, J., Ervasti, J. M., Bergmann, C., Tiemeyer, M., and Wells, L. (2010) Site mapping and characterization ofO-glycan structures on α-dystroglycan isolated from rabbit skeletal muscle. J. Biol. Chem. 285, 24882-24891
49. Nilsson, J., Nilsson, J., Larson, G., and Grahn, A. (2010) Characterization of site-specific O-glycan structures within the mucin-like domain of α-dystroglycan from human skeletal muscle. Glycobiology 20, 1160-1169
50. Stalnaker, S. H., Aoki, K., Lim, J. M., Porterfield, M., Liu, M., Satz, J. S., Buskirk, S., Xiong, Y., Zhang, P., Campbell, K. P., Hu, H., Live, D., Tiemeyer, M., and Wells, L. (2011) Glycomic analyses of mouse models of congenital muscular dystrophy. J. Biol. Chem. 286, 21180-21190
51. Chiba, A., Matsumura, K., Yamada, H., Inazu, T., Shimizu, T., Kusunoki, S., Kanazawa, I., Kobata, A., and Endo, T. (1997) Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve α-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in the binding of α-dystroglycan with laminin. J. Biol. Chem. 272, 2156-2162
52. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S. H., Davis, S., Kunz, S., Madson, M., Oldstone, M. B., Schachter, H., Wells, L., and Campbell, K. P. (2010) O-Mannosyl phosphorylation of α-dystroglycan is required for laminin binding. Science 327, 88-92
53. Inamori, K., Yoshida-Moriguchi, T., Hara, Y., Anderson, M. E., Yu, L., and Campbell, K. P. (2012) Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science 335, 93-96